Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch

Songbirds learn and maintain their songs via auditory experience. Neurons i n many telencephalic nuclei important to song production and development ar e song selective, firing more to forward auditory playback of the bird's ow n song (BOS) than to reverse BOS or conspecific songs. Elucidating circuits that generate these responses can localize where auditory experience influ ences vocalization, bridging cellular and systems analyses of song learning . Song-selective responses in many song nuclei, including the vocal premoto r nucleus robustus archistriatalis (RA) and the basal ganglia homolog area X, are thought to originate in nucleus HVc (used as a proper name), which c ontains interneurons and relay cells that innervate either RA or area X. Pr evious studies indicated that only X-projecting neurons have auditory respo nses, leaving open the source of RA's auditory input and the degree to whic h song selectivity may be refined in HVc. Here, in vivo intracellular recor dings from morphologically and electrophysiologically identified HVc neuron s revealed that both relay cell types fire song-selectively. However, their firing arises via markedly different subthreshold processes, and only X-pr ojecting neurons appear to be sites for auditory refinement. RA-projecting neurons exhibited purely depolarizing subthreshold responses that were high ly song selective and that were excitatory. In contrast, subthreshold respo nses of X-projecting neurons included less-selective depolarizing and highl y selective hyperpolarizing components. Within individual birds, these BOS- evoked hyperpolarizations closely matched interneuronal firing, suggesting that HVc interneurons make restricted inputs onto X-projecting neurons. Bec ause of the two relay cell types' subthreshold differences, factors affecti ng their resting membrane potentials could enable them to transmit distinct song representations to their targets.